Crohn’s disease: review and standardization of nomenclature

Crohn’s disease is an inflammatory bowel disease that can affect any segment of the gastrointestinal tract. It has a variable clinical course, with alternating periods of disease activity and remission. Because the incidence and prevalence of Crohn’s disease have been increasing, evaluation by imaging methods has become more important. The most widely used methods are computed tomography enterography, magnetic resonance enterography (as an elective examination), and contrast-enhanced computed tomography (in the context of emergency). Computed tomography enterography and magnetic resonance enterography are useful for diagnosis, follow-up, evaluation of complications, and prognosis. Both can be used in order to evaluate the small bowel loops and the associated mesenteric findings, as well as to evaluate other abdominal organs. They both also can detect signs of disease activity, fibrosis, penetrating disease, and complications. The interpretation of such changes is essential to the multidisciplinary approach, as is the standardization of the nomenclature employed in the reports. In this paper, we review and illustrate the imaging findings of Crohn’s disease, using the standardized nomenclature proposed in the multidisciplinary consensus statement issued by the Society of Abdominal Radiology, the Society of Pediatric Radiology, and the American Gastroenterology Association, with recommendations for descriptions, interpretations, and impressions related to those findings.


INTRODUCTION
Crohn's disease is an inflammatory bowel disease that can affect any segment of the gastrointestinal tract, from the mouth to the anus. The clinical course is varied, alternating between periods of disease activity and remission. The incidence and prevalence of inflammatory bowel diseases have been increasing worldwide, and their importance has therefore been growing (1) . There has been a significant improvement in the survival of patients with these of 40 min and contains neutral enteric contrast (3% polyethylene glycol or mannitol) diluted in 1.5 L of water (4) .
Because it requires only a short breath hold, CTE is a rapid test and is therefore well tolerated by uncooperative patients. In comparison with MRE, CTE has greater reproducibility, is more widely availability, provides greater spatial resolution, and is more easily evaluated by general radiologists. However, it has a lower capacity for tissue characterization and less capacity to differentiate between fibrosis and disease activity. In addition, CTE uses ionizing radiation, which can be harmful to patients with Crohn's disease, who are typically young and undergo many tests throughout their lives (4,5) .
In comparison with CTE, MRE is a longer examination and requires greater patient cooperation because the protocol calls for multiple breath holds. In addition, it requires a 1.5-T or 3.0-T scanner to acquire good quality images. Therefore, MRE is less reproducible. Because of its higher cost and limited availability, MRI is, in general, less accessible than is CT. However, it is a technique that allows greater tissue resolution, making it the better method for differentiating between disease activity and fibrosis. Dynamic (cine) MRI allows the evaluation of peristalsis, increasing the accuracy of the method for detecting strictures, inflammation, and fibrosis. Furthermore, the use of multiple sequences provides a higher degree of confidence regarding enteric and perienteric alterations, with fewer false-positive and false-negative results. That also allows better characterization of fistulas and abscesses, as well as of other complications. Moreover, MRI does not use ionizing radiation and can be repeated multiple times, even in children (4) .
An evaluation employing the combination of CTE and ileocolonoscopy to observe Crohn's disease activity has been shown to have a sensitivity of 84% and a specificity of 94% (6) . However, patients may not show changes in the segments evaluated by ileocolonoscopy, the results of which can be normal in cases in which the disease spares the colon, ileocecal valve, and distal ileum, making it even more important to complement it with other cross-sectional imaging methods that allow evaluation of the gastrointestinal tract as a whole (6) .
Endoscopy is also unable to assess the response to treatment in the submucosal layer, muscle, and adjacent structures. In addition to allowing an evaluation of the response to treatment in the intestinal wall, perienteric fat, and adjacent structures, MRE is also better than is CTE in differentiating between disease activity and fibrosis, which facilitates the individualization of treatment (7) . The main differences between CTE and MRE are presented in Table 1.
In the emergency department, patients with Crohn's disease often present with intestinal distention typical of the underlying disease or its complications and do not tolerate the preparation for CTE. In such cases, CT examination with intravenous contrast administration is indicated. The intestinal distention already presented by the patient may be sufficient for the diagnosis. Contrast-enhanced CT is the imaging method most often used in the emergency department. In addition, CT can be used in order to evaluate the complications of Crohn's disease, such as inflammatory masses, collections, fistulas, and perforations. It can also facilitate the differential diagnosis between abdominal pain related to Crohn's disease activity and that related to other diagnoses, such as acute diverticulitis, acute appendicitis, acute cholecystitis, pancreatitis, mesenteric ischemia, and neoplasia. Furthermore, CT can be used in guiding interventional procedures, such as the drainage of fluid collections and intra-abdominal abscesses (4,5,8) .
There is currently a need to standardize the terminology used in radiology reports, to improve multidisciplinary understanding and the individualization of the treatment of Crohn's disease. One valuable resource is the 2018 consensus statement on nomenclature authored by representatives of the Society of Abdominal Radiology, the Society of Pediatric Radiology, and the American Association of Gastroenterology, together with other experts on the subject (9,10) .

Inflammation-related findings
Segmental mural hyperenhancement -This is defined as increased attenuation and increased signal in the various enteric (mural) layers on contrast-enhanced CT and MRI examinations, respectively. It is evaluated in the enteric phase (45-50 s after intravenous contrast administration) or in the venous phase (60-70 s after intravenous contrast administration), and the accuracy is similar in both phases (11) . Mural hyperenhancement can be classified as asymmetric, stratified, or homogeneous (9-11) .
• Asymmetric hyperenhancement is specific to Crohn's disease and mainly involves the mesenteric border of the bowels ( Figure 1A).
• Stratified hyperenhancement is defined as enhancement of the inner layer of the loop (bilaminar hyperen- Does not use ionizing radiation hancement) or of the inner and outer layers (trilaminar hyperenhancement; Figure 1B). The term "mucosal enhancement" should be avoided, because when enhancement of the inner layer is observed, the mucosa is no longer individualized on endoscopy. Stratified hyperenhancement can be associated with edema, granulation tissue, fat deposition, wall fibrosis, or inflammation.
• Homogeneous hyperenhancement is defined as enhancement involving all layers of the bowel uniformly ( Figure 1C). It is less specific and can be due to fibrosis, intestinal ischemia, or collagen deposition.
Segmental wall thickening -The thickest wall of the most inflamed segment should be measured, with good distension of the loop. Such thickening is classified as mild if the wall thickness is 3-5 mm ( Figure 1C), moderate if it is 5-10 mm ( Figure 2A) and severe if it is > 10 mm ( Figure   2B). A wall thickness > 15 mm, especially if asymmetrical, is not an expected finding and should raise the suspicion of neoplasia (9)(10)(11) .
Wall edema -This is defined as greater attenuation on CT and as high signal intensity on T2-weighted MRI sequences with or without fat suppression. On T2-weighted sequences without fat suppression, the differential diagnosis with fat deposition in the wall of a bowel loop, which also shows a hyperintense signal, is worthy of consideration. On T2-weighted sequences with fat suppression, the edema maintains the hyperintense signal and the fat shows a hypointense signal (9)(10)(11) .
Stenosis -This is characterized as a ≥ 50% reduction in luminal diameter in comparison with that of the adjacent loop, together with unequivocal upstream dilation of the same loop (> 3 cm in caliber). Stenosis is most often seen

A B
in patients with active infl ammation, although fi brosis and infl ammation are often both present, in which case the infl ammation leads to fi brosis and the fi brosis leads to infl ammation, in a feedback loop. In cases of stenosis, penetrating disease should also be evaluated, because there is a mechanism of high pressure and infl ammation, often causing fi stulization proximal to the stenosis (9-11) . The extent of the stenotic segment and the caliber of the upstream dilatation should be described in the report. Figure 3A shows probable stenosis, with negligible (< 3 cm) dilatation, Figure 3B shows stenosis with mild (3-4 cm) dilatation, and Figure 3C shows stenosis with marked (≥ 4 cm) dilatation (9)(10)(11) .
Ulceration -This is defi ned as a discontinuity of the inner wall of the bowel loop, with penetration of the luminal contents into the wall of the loop. It is an indicator of severe disease activity (9-11) .
Restricted diffusion -When there is infl ammation, the wall of the bowel loops show restricted diffusion, increasing the sensitivity for detecting more subtle changes, which must be confi rmed in the rest of the examination. However, luminal content and undistended loops can also show restricted diffusion. Therefore, diffusion-weighted sequences should always be interpreted together with the other sequences (9-11) .
Outpouchings -These are defi ned as sac-like dilatations of the antimesenteric border of the bowel loop, resulting from acute or chronic infl ammation with fi brosis at the mesenteric border (9-11) .
Reduced loop motility -Cine MRE sequences can detect reduced peristalsis in bowel loops that are infl amed, fi brotic, or both. The reduction in peristalsis is proportional to the degree of infl ammation and fi brosis (9)(10)(11)(12) .

Findings related to penetrating disease
Sinus tract -This is defi ned as a discontinuity of the bowel loop wall, extending to the perienteric fat, with a blind-ending, without reaching the surrounding structures or the skin (9-11) , as illustrated in Figure 4.
Simple and complex fistulas -A simple fi stula is defi ned as a single extraenteric tract that connects a bowel loop with another loop or an adjacent organ ( Figure 5). Complex fi stulas are defi ned as multiple tracts connecting bowel loops with other loops or adjacent organs ( Figure  6). Fistulas occur when there is active infl ammation. The shape of a complex fi stula can be described as a cloverleaf, asterisk, or star (9)(10)(11) .
Inflammatory mass -This term refers to ill-defi ned infl ammation of the fat, without a wall and without an organized liquid component, adjacent to a loop in which there is active infl ammation (9)(10)(11) .
Abscess -This is defi ned as a fl uid collection with a well-defi ned wall that enhances on contrast-enhanced images and content that shows restricted diffusion, adjacent to a loop in which there is active infl ammation (9-11) .

Mesenteric fi ndings related to Crohn's disease
Perienteric edema or inflammation -Increased attenuation of perienteric fat on CTE or a hyperintense signal on T2-weighted MRE, adjacent to a loop in which there is active infl ammation. Perienteric edema occurs when infl ammation extends into the perienteric space (9-11) , as depicted in Figure 8.  Free perforation - Figure 7 shows an example of bowel loop perforation with active infl ammation and free intraperitoneal air, which necessitates surgical evaluation (9-11) .   Engorged vasa recta -Increased blood supply and drainage of a small bowel loop segment (Figure 9), due to active inflammation, results in engorgement of the vasa recta, also known as the comb sign (9)(10)(11) .
Fibrofatty proliferation -This is defined as hypertrophy of the perienteric fat adjacent to a bowel loop segment with long-term involvement by Crohn's disease, detaching the loop from the neighboring structures ( Figure 10). Such proliferation is a sign of chronicity (9)(10)(11) .
Reactive lymphadenopathy -This is defined as reactive lymph nodes, with a short-axis diameter of 1.0-1.5 cm, corresponding to a bowel loop in which there is active inflammation (9-11) .

Extraintestinal manifestations of Crohn's disease
As detailed in Table 2, the clinically relevant manifestations of Crohn's disease include primary sclerosing cholangitis, pancreatitis, avascular necrosis, and sacroiliitis (9)(10)(11) . In its early stages, primary sclerosing cholangitis can often be identified on enterography as small focal dilatations of the intrahepatic bile ducts, and evaluation of the bile ducts by magnetic resonance cholangiopancreatography is indicated (13) . The main causes of pancreatitis in patients with Crohn's disease are gallstones and pharmacological treatment, especially with azathioprine and mesalazine (14) , as well as with glucocorticoids and some other medications (15) . In such patients, pancreatitis typically has a mild or moderate clinical presentation and responds well after the end of treatment. Avascular necrosis mainly affects the femoral head, presenting clinically as hip pain. Sacroiliitis often manifests with low back pain as its main symptom, as confirmed by findings of (typically asymmetric) discrete erosions or even fusion of the sacroiliac joint (16) .

STRUCTURED REPORT
The radiology report should present the important information in a systematic manner (Table 3), in order to improve the quality and reproducibility of the communication with the multidisciplinary team. It is also important to provide a clear impression regarding inflammation, fibrosis, penetrating disease, and secondary involvement of distant structures (9-11) .

Chronic mesenteric venous occlusion -This occurs
when there is occlusion of the collateral mesenteric vessels in segments of a bowel loop in which there is inflammation. In acute cases, in which the mesenteric vessels are typically distended by a thrombus, the term "thrombosis" should be used. In chronic cases, that term should not be used, because it could lead to the unnecessary use of anticoagulants. In such cases, the preferred term is "occlusion". In cases of chronic mesenteric venous occlusion, the central mesenteric veins are narrowed ( Figure 11) (9-11) .

TERMS TO AVOID IN THE FINAL REPORT
As established in the 2018 consensus, certain terms are no longer used (Table 4).

CONCLUSION
In individuals with Crohn's disease, CTE and MRE are valuable tools for diagnosis, assessment of the extent of the disease and its complications, as well as of associated conditions, facilitating the selection of the best clinical and surgical treatments, as well as the differential diagnoses. The structured radiology report allows the systematic evaluation of all structures and alterations to be described in Crohn's disease and facilitates the follow-up of patients with the disease.

Nephrolithiasis
Can affect the entire bile duct and presents with multiple strictures and intrahepatic dilatations or mural thickening of the extrahepatic bile duct, with contrast enhancement and without upstream dilation Focal sclerosis of the anterior portion of the femoral head, best visualized in the coronal plane Discrete bone erosions at sacroiliac joint fusion; high signal intensity on T2-weighted MRE sequences; subchondral edema; contrast enhancement; usually asymmetric but can affect the joint bilaterally Consequent to cholelithiasis or pharmacological treatment Thought to result from inadequate reabsorption of bile salts (16) Occurs in patients with diarrheal disease and ileal involvement; has a pathophysiological relationship with the formation of kidney stones (17) Table 3-Terms to be used in the impression section of the radiology report.